Evolution of the ABPA Subunit of Androgen-Binding Protein Expressed in the Submaxillary Glands in New and Old World Rodent Taxa

The salivary androgen-binding proteins (ABPs) are members of the secretoglobin gene family present in mammals. Each ABP is a heterodimer assembled as an ABPA subunit encoded by an Abpa gene and linked by disulfide bridges to an ABPBG subunit encoded by an Abpbg gene. The ABP dimers are secreted into the saliva of mice and then transferred to the pelage after grooming and subsequently to the environment allowing an animal to mark territory with a biochemical signal. The putative role of the mouse salivary ABPs is that of pheromones mediating mate selection resulting in assortative mating in the Mus musculus species complex. We focused on comparing patterns of molecular evolution between the Abpa genes expressed in the submaxillary glands of species of New World and Old World muroids. We found that in both sets of rodents the Abpa genes expressed in the submaxillary glands appear to be evolving under a similar evolutionary regime, with relatively high nonsynonymous substitution rates, suggesting that ABP might play a similar biological role in both systems. Thus, ABP could be involved with mate recognition and species isolation in New World as well as Old World muroids.     

The mouse salivary androgen-binding protein (ABP) alpha subunit closely resembles chain 1 of the cat allergen Fel dI

Androgen-binding protein (ABP) is found in the salivas of a wide variety of rodents and it has been proposed that ABP functions in sex and/or subspecies recognition (Karn and Dlouhy,J. Hered. 82, 453, 1991). This is a report of significant identity between the alpha subunit of mouse salivary ABP and Chain 1 of cat allergen Fel dI (50% identity), as well as with two other proteins that share identity with Chain 1 of Fel dI, rabbit uteroglobin (27% identity with ABP alpha) and human lung Clara 10 (27% identity with ABP alpha). The secondary structure predicted for the mouse ABP alpha subunit is a very good fit with the secondary structure determined by X-ray crystallography for rabbit uteroglobin, a protein that shares with mouse ABP the capability of binding steroid. Fel dI is found in cat saliva, sebaceous glands, and pelt. Its function is not known but it has been proposed to be involved in protecting dry epithelia, a parallel to uteroglobin protecting wet epithelia. Since mice, like cats, lick themselves and each other extensively, coating their pelts with ABP may be part of this or another biological function.     

Do male house mice (Mus musculus) discriminate between females that differ in nutritional status?

Most studies of mate choice have focused on female preference for male traits because it is generally assumed that since males provide less parental investment they are not choosy. However, if males suffer missed opportunity costs by mating with lower quality females, selection should favor males with the ability to discriminate among females. We tested the hypothesis that male house mice (Mus musculus) discriminate between females that differ in nutritional status (non-food-deprived versus food-deprived). We recorded the time males spent investigating either type of female and used that to determine preference (spending ≥55% of their total investigation time with one female). We also examined the effects of female nutritional status and female preference status (preferred versus non-preferred) on the reproductive success of males. Males did not display a preference for non-food-deprived females nor did their reproductive success vary with nutritional status or preference status of females. Interestingly, males spent more time investigating females that were closest to the male's own weight. In addition, pairs that were closer in weight were more likely to produce a litter. These results suggest that male house mice are capable of discriminating among females and that such discrimination may influence their reproductive success.     

Reinforcement selection acting on the European house mouse hybrid zone

Behavioural isolation may lead to complete speciation when partial postzygotic isolation acts in the presence of divergent‐specific mate‐recognition systems. These conditions exist where Mus musculus musculus and M. m. domesticus come into contact and hybridize. We studied two mate‐recognition signal systems, based on urinary and salivary proteins, across a Central European portion of the mouse hybrid zone. Introgression of the genomic regions responsible for these signals: the major urinary proteins (MUPs) and androgen binding proteins (ABPs), respectively, was compared to introgression at loci assumed to be nearly neutral and those under selection against hybridization. The preference of individuals taken from across the zone regarding these signals was measured in Y mazes, and we develop a model for the analysis of the transition of such traits under reinforcement selection. The strongest assortative preferences were found in males for urine and females for ABP. Clinal analyses confirm nearly neutral introgression of an Abp locus and two loci closely linked to the Abp gene cluster, whereas two markers flanking the Mup gene region reveal unexpected introgression. Geographic change in the preference traits matches our reinforcement selection model significantly better than standard cline models. Our study confirms that behavioural barriers are important components of reproductive isolation between the house mouse subspecies.     

The mouse salivary androgen-binding protein (ABP) gene cluster on Chromosomes 7: characterization and evolutionary relationships

Mouse salivary androgen-binding protein (ABP) is a pair of dimers, composed of an alpha subunit disulfide bridged to either a beta or a gamma subunit. It has been proposed that each subunit is encoded by a distinct gene: Abpa, Abpb, and Abpg for the alpha, beta, and gamma subunits, respectively. We report here the structures and sequences of the genes that encode these three subunits. Each gene has three exons separated by two introns. Mouse salivary ABP is a member of the secretoglobin family, and we compare the structure of the three ABP subunit genes to those of 18 other mammalian secretoglobins. We map the three genes as a gene cluster located 10 cM from the centromere of Chromosome (Chr) 7 and show that Abpa is the closest of the three to the gene for glucose phosphate isomerase (GPI) and that Abpg is the closest to the centromere, with Abpb mapping between them. Abpa is oriented in the opposite direction to Abpb and Abpg, with its 5 end directed toward their 5 ends. We compare the location of these genes with other secretoglobin genes in the mouse genome and with the known locations of secretoglobin genes in the human genome and present evidence that strong positive selection has driven the divergence of the coding regions of Abpb and Abpg since the putative duplication event that created them. The nucleotide sequence data reported in this paper have been submitted to GenBank and have been assigned the accession numbers Abpa: AF144714; Abpb: AY325897; Abpg: 325898. *Current address: (Christina M. Laukaitis) Department of Internal Medicine, St. Vincent Hospital, 2100 W. 86th St., Indianapolis, IN 46260, USA     

Female Mate Preference for Males Having Long and Symmetric Fins in the Bower-holding Cichlid Cyathopharynx furcifer

Female mate preference in a bower-holding cichlid, Cyathopharynx furcifer, was studied in Lake Tanganyika. Most males held territories with crater-shaped bowers in sand, but some males held territories without bowers. Territories were distributed adjacently and females visited them to spawn. After engaging in circling behaviour with the male, a female deposited eggs in the bower. Soon after spawning, the female picked the eggs up into her mouth and brooded them in places away from male territories. Female mate choice appeared to follow three steps: 1) females visited only bower-holding male territories, and more frequently visited territories of males that performed courtship displays at a higher frequency and had longer pelvic fins; 2) females preferred to start circling with males having longer and more symmetrical pelvic fins; 3) females chose males with more symmetrical pelvic fins as their mates. Less than 7% of females that visited male territories spawned eggs in the bowers. In contrast to other bower-holding species, bower size did not correlate with male reproductive success in C. furcifer. Bowers may therefore be essential as spawning sites or may function as a species recognition character for females. Female choice may be dependent instead on males having long and symmetrical pelvic fins apparent during the circling behaviour carried out in the bowers.     

A ROLE FOR LEARNING IN POPULATION DIVERGENCE OF MATE PREFERENCES

Learning and other forms of phenotypic plasticity have been suggested to enhance population divergence. Mate preferences can develop by learning, and species recognition might not be entirely genetic. We present data on female mate preferences of the banded demoiselle (Calopteryx splendens) that suggest a role for learning in population divergence and species recognition. Populations of this species are either allopatric or sympatric with a phenotypically similar congener (C. virgo). These two species differ mainly in the amount of wing melanization in males, and wing patches thus mediate sexual isolation. In sympatry, sexually experienced females discriminate against large melanin wing patches in heterospecific males. In contrast, in allopatric populations within the same geographic region, females show positive (“open‐ended”) preferences for such large wing patches. Virgin C. splendens females do not discriminate against heterospecific males. Moreover, physical exposure experiments of such virgin females to con‐ or hetero‐specific males significantly influences their subsequent mate preferences. Species recognition is thus not entirely genetic and it is partly influenced by interactions with mates. Learning causes pronounced population divergence in mate preferences between these weakly genetically differentiated populations, and results in a highly divergent pattern of species recognition at a small geographic scale.     

Territorial and mating behavior ofXylocopa fimbriata F. andXylocopa gualanensis Cockerell from Costa Rica

The territorial and mating behavior of two Xylocopaspecies X. fimbriataF. and X. gualanensisCockerell from Costa Rica are described. Male territorial activity was common during February through April in the higher areas of a dry forest savanna. Both species maintained territories at the same location within hollows in the foliage of Ardesia revolutaH.B.K., a small evergreen tree which occurs commonly in the dry forest. Xylocopa fimbriatamaintained territories during early morning hours, whereas the territorial period for X. gualanensisoccurred during late afternoon. Males of both species infrequently marked territories. It is suggested that a secretion released from their mesosomal glands is wiped onto their legs during frequent leg-body and leg rubbing which occurs while males hover. The secretion is occasionally applied to marking points on vegetation by their secretion-contaminated legs. Males repeatedly marked select locations when females were near their territories regardless of whether females were searching nearby branches for nesting sites, gathering provisions, or passing through their areas. Some females oriented to and entered certain male territories. An example of female mate choice in selection of male territories is provided. Females flew into male territories from 2–4 cm down-wind of male scent-marked locations. As females approached these locations, males hovered downwind in close proximity to the females' approach path. As females hovered a few centimeters downwind of the scented focal point, males approached from downwind and mounted. The males behavior and the role of scent-marking in the reproductive behavior of lek polygyny is discussed.     

Interspecific interactions and learning variability jointly drive geographic differences in mate preferences

Co‐occurrence of closely related species can cause behavioral interference in mating and increase hybridization risk. Theoretically, this could lead to the evolution of more species‐specific mate preferences and sexual signaling traits. Alternatively, females can learn to reject heterospecific males, to avoid male sexual interference from closely related species. Such learned mate discrimination could also affect conspecific mate preferences if females generalize from between species differences to prefer more species‐specific mating signals. Female damselflies of the banded demoiselle (Calopteryx splendens) learn to reject heterospecific males of the beautiful demoiselle (C. virgo) through direct premating interactions. These two species co‐occur in a geographic mosaic of sympatric and microallopatric populations. Whereas C. virgo males have fully melanized wings, male C. splendens wings are partly melanized. We show that C. splendens females in sympatry with C. virgo prefer smaller male wing patches in conspecific males after learning to reject heterospecific males. In contrast, allopatric C. splendens females with experimentally induced experience with C. virgo males did not discriminate against larger male wing patches. Wing patch size might indicate conspecific male quality in allopatry. Co‐occurrence with C. virgo therefore causes females to prefer conspecific male traits that are more species specific, contributing to population divergence and geographic variation in female mate preferences.     

Female defense polygyny in the territorial triggerfish <Emphasis Type="Italic">Sufflamen chrysopterum</Emphasis>

The occurrence of polygyny requires specific environmental conditions such as female aggregation or patchy resource distribution. However, it is difficult to determine the factors responsible for polygyny in species in which the territories of both sexes overlap. To overcome this, we performed female removal experiments in the polygynous triggerfish Sufflamen chrysopterum (Balistidae) in the Okinawa coral reef. Both sexes defended their territories exclusively against consexuals of the same species, and female aggregation was absent. Each male territory included 1–3 female territories, and nonterritorial males were significantly smaller than territorial males. Further, the body size of territorial males was positively correlated with that of the largest female in their territories, and larger males tended to mate with more females. The results of the female removal experiments (n = 10 females) indicated that females competed for better territories rather than larger mates. In contrast, males abandoned the territories once the females emigrated. These results strongly suggest that males defend females rather than sites and compete for larger and a greater numbers of females. Thus, in S. chrysopterum, female defense polygyny occurs in the absence of female aggregation.     

Females benefit from multiple mating but not multiple mates in the burying beetle Nicrophorus vespilloides

Male reproductive success generally increases with number of mates but this need not be true for females. If females are the limiting sex, as few as one mate can be optimal. Despite the theoretical differences driving multiple mating in the sexes, multiple mating is the norm rather than the exception. Empirical investigations are therefore required to determine why females mate with multiple males. Both nonadaptive (correlated responses to selection on males, given the mean mating rates have to be the same) and adaptive (direct or indirect fitness benefits) can drive the evolution of multiple mating in females. Females of the burying beetle Nicorphorus vespilloides often mate repeatedly with the same male, but this appears to be a correlated response to selection on males rather than reflecting direct benefits to females for multiple mating. However, an unexamined alternative to this nonadaptive explanation is that females benefit by mating with multiple different males and therefore are selected for general promiscuity. Here we examine if mating polyandrously provides fitness benefits by examing the effects of number of mates (1, 2 or 3), mating system (monogamous, polyandrous) and their interaction. The only significant influence was mating more than once. This did not depend on type of mating. We suggest that unlike most other species examined, in N. vespilloides mating with the same male repeatedly or with several different males reflects an indiscriminate willingness to mate as a result of correlated selection on males for high rates of mating.     

Limited indirect fitness benefits of male group membership in a lekking species

In group living species, individuals may gain the indirect fitness benefits characterizing kin selection when groups contain close relatives. However, tests of kin selection have primarily focused on cooperatively breeding and eusocial species, whereas its importance in other forms of group living remains to be fully understood. Lekking is a form of grouping where males display on small aggregated territories, which females then visit to mate. As females prefer larger aggregations, territorial males might gain indirect fitness benefits if their presence increases the fitness of close relatives. Previous studies have tested specific predictions of kin selection models using measures such as group‐level relatedness. However, a full understanding of the contribution of kin selection in the evolution of group living requires estimating individuals' indirect fitness benefits across multiple sites and years. Using behavioural and genetic data from the black grouse (Tetrao tetrix), we show that the indirect fitness benefits of group membership were very small because newcomers joined leks containing few close relatives who had limited mating success. Males' indirect fitness benefits were higher in yearlings during increasing population density but marginally changed the variation in male mating success. Kin selection acting through increasing group size is therefore unlikely to contribute substantially to the evolution and maintenance of lekking in this black grouse population.     

Experimental evidence for female choice and energetic costs of male tail elongation in red-collared widowbirds

The black nuptial plumage of the highly polygynous male red‐collared widowbird (Euplectes ardens) comprises a red carotenoid‐based collar patch and a long graduated tail (c. 22 cm). Tail length was the strongest predictor of male mating success in a previous selection analysis, motivating this experimental test of the relative importance of tail plumes in male contest competition and female choice. Males were assigned to either a short (12.5 cm) or control (20 cm) tail manipulation prior to territory establishment. Male contest competition was unaffected by the tail treatments as the shortened‐ and control‐tailed males were equally successful in acquiring territories of similar size and quality. In contrast, however, although the longer‐tailed control males spent less time in flight and courtship displays, they attracted significantly more prospecting and nearly three times as many nesting females to their territories compared to the short‐tailed males. In further support of tail length as the primary mate choice cue, none of the other measured and potential female cues (e.g. body size, collar colorimetrics, territorial behaviours or territory quality) influenced male reproductive success. In addition to potentially increasing detectability (‘signal efficacy’), the long tail is also a likely indicator of male quality (‘signal content’). Despite the higher activities of short‐tailed males, control‐tailed males showed a steeper decline in condition (relative body mass) during the breeding season. Furthermore, both short‐ and control‐tailed residents lost more condition than did the short‐ and control‐treated floaters (males not establishing territories), suggesting an interaction between tail length and the costs of territory acquisition, defence and courtship displays. These results confirm the role of mate choice and honest quality advertising as the main selection pressures behind elongated tails in widowbirds. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 86 , 35–43.     

Reproductive character displacement of female mate preferences for male cuticular hydrocarbons in Drosophila subquinaria

Several lines of evidence implicate sexual isolation in both initiating and completing the speciation process. Although its existence is straightforward to demonstrate, understanding the evolution of sexual isolation requires identifying the underlying phenotypes responsible so that we can determine how these have diverged. Here, we study geographic variation in female mate preferences for male sexual displays in the fly Drosophila subquinaria. Female D. subquinaria that are sympatric with its sister species D. recens discriminate strongly against both D. recens and allopatric conspecific males, whereas females from allopatric populations do not. Furthermore, female mate preferences target at least in part a suite of cuticular hydrocarbons (CHCs) in males and geographic variation in CHCs mirrors the pattern of mate discrimination. In this study, we quantify female mate preferences for male CHCs from populations that span the geographic range of D. subquinaria. We find that the direction of linear sexual selection varies significantly between populations that are sympatric versus allopatric with D. recens in a pattern of reproductive character displacement. Differences in preference partially align with existing differences in CHCs and patterns of sexual isolation, although discrepancies remain that suggest the involvement of additional traits and/or more complex, nonlinear preference functions.     

Males,but not females,perform strategic mate searching movements between host plants in a leaf beetle with scramble competition polygyny

Mate searching is assumed to be performed mostly by males, but when females benefit from multiple mating or are under risk of failing to mate, they may also perform mate searching. This is especially important in scramble competition polygynies, in which mate searching is the main mechanism of mate competition. Typically, more mobile individuals are expected to achieve higher mating success because mobility increases their probability of finding mates. If we assume individual movements are mainly explained by mate searching in scramble competition polygynies, we can investigate searching strategies by asking when individuals should leave their location and where they should go. We hypothesize that individuals will leave their locations when mating opportunities are scarce and will seek spatially close sites with better mating opportunities. We tested these hypotheses for males and females of Leptinotarsa undecimlineata, a leaf beetle with scramble competition polygyny in which both sexes are promiscuous. Individuals mate and feed exclusively on Solanum plants, and thus, individual movements can be described as switches between plants. Females were less likely than males to leave isolated plants, and both males and females moved preferentially to neighboring plants. Males were more likely to leave when the local number of females was low, and the number of males was high. They moved to plants with more females, a behavior consistent with a mate searching strategy. Females were more likely to move to plants with fewer males and many females, a behavior consistent with male harassment avoidance. Strategic movement is widely considered in foraging context, but seldom in a mate searching context. Considering that selection to minimize searching costs, maximize mating success, and minimize harassment may be ubiquitous in nature, we argue that strategic movements by mate searching individuals are likely to occur in many species.     

Female discrimination thresholds frequently exceed local male display variation: implications for mate choice dynamics and sexual selection

Among the factors that can influence female mate choice decisions is the degree to which females differentiate among similar displays: as differences decrease, females are expected to eventually stop discriminating. This discrimination threshold, in conjunction with the magnitude of male trait variation females regularly encounter while making mate choice decisions, may have important consequences for sexual selection. If local display variation is above the discrimination threshold, female preferences should translate into higher mating success for the more attractive male. But if display variation is frequently below the threshold, the resulting increased pattern of random mating may obscure the existence of female mate choice. I investigated the interplay between female discrimination and male display variation in green treefrogs (Hyla cinerea) and found that call trait differences between nearest neighbour males were frequently smaller than what females are expected to discriminate. This finding has two important consequences for our understanding of sexual selection in the wild: first, low display variation should weaken the strength of selection on male display traits, but the direction of selection should mirror the one predicted from females choice trials. Second, caution is needed when interpreting data on realized mating success in the wild: a pattern of random mating with respect to male display traits does not always mean that female preferences are weak or that conditions are too challenging for females to express their preferences. Rather, insufficient display variation can generate the same pattern.     

Female preference for male saliva: implications for sexual isolation of Mus musculus subspecies

We studied the effects of a single genetic change on a complex mammalian behavior using animals congenic for two variants of Abpa, the gene for the alpha subunit of mouse salivary androgen-binding protein (ABP), in two-way preference tests. Females exhibited a preference for investigating salivas of males of their own genetic type of ABP but not for urines of either type of male. This preference behavior is consistent for samples of mice from geographically diverse populations of Mus musculus domesticus and M. m. musculus. These findings provide an explanation for the observation that this gene is evolving under strong selection.     

Mate Choice by Both Sexes Maintains Reproductive Isolation in a Species Flock of Pupfish (Cyprinodon spp) in the Bahamas

Female and male mate choices can reinforce reproductive isolation after sympatric speciation. Using a binary choice design, we examine the importance of visual cues in female mate choice in all three sympatric species of pupfish on San Salvador Island. We also examine the importance of olfactory cues in female choice of the hard‐shelled invertebrate specialist (Cyprinodon brontotheroides). We examine male mate choice in two of the three species, the scale eater (C. desquamator) and the detritivore (C. variegatus). Females of all three species use visual cues and prefer conspecific males. C. brontotheroides females do not use olfactory cues to discriminate between conspecific and heterospecific males. Males of C. desquamator and C. variegatus also preferentially court conspecific females. Thus, mutual mate choice, where both females and males exhibit mate choice, acts as a strong behavioral pre‐mating isolation mechanism in these sympatrically speciated pupfish.     

Common Wall Lizard Females (Podarcis muralis) do not Actively Choose Males Based on their Colour Morph

Identifying the processes that lead to the evolution and maintenance of links between colour morphs and behavioural strategies has implications for the evolution of reproductive isolation and sympatric speciation. Sexual selection may play a significant role in the evolution of colour pattern complexity in reptiles, particularly when there are fitness consequences associated with mating with males of different colour morphs. In this article, we explored if common wall lizard females (Podarcis muralis) actively select males according to their morph in a colour‐assortative pattern using a multiple‐choice experiment with both visual and chemical cues. We failed to identify female active mate choice, as females did not choose males based on male colouration or femoral pore secretions. Indeed, females equally entered the three preference compartments and spent nearly the same amount of time within them, irrespective of both colour and odour of males. Consequently, our results do not support the hypothesis that colour polymorphism in this species may be driven by colour‐assortative mating promoted by females. However, we cannot exclude the possibility that females may choose males according to their colour following a flexible choice strategy, nor the possibility that females actively discriminate among males according to qualities that are not directly related to morph‐specific strategies.     

Mate discrimination by females in the burying beetle Nicrophorus orbicollis: the influence of male size on attractiveness to females

1. Female burying beetles behave differently towards males of different sizes, avoiding mating with large males that are not defending resources but mating with small males regardless of the presence of resources. Females of the burying beetle Nicrophorus orbicollis were therefore examined to determine whether they discriminate among males using only pheromonal signals. The influence of female size on its own mate choice was also examined. 2. Females do use male pheromonal signals to discriminate among males and these signals do appear to convey information about male body size to females. Overall, females were more likely to be attracted to larger males than to smaller males. 3. Female choice of a male was influenced by both the female's own body size and the size of the female relative to the size of the two males available to it. 4. While there is an overall mating advantage for larger males, resulting from female preferences based on odour cues, smaller males are also attractive to some females under some circumstances. 5. It is argued that there are different costs and benefits of mating with different sized males, leading to the evolution of context‐dependent mate choice for females and the need to be able to discriminate males of different sizes from a distance.